Occurrence and Habitats of the Giant Mottled Eel Anguilla marmorata (Anguilliformes, Anguillidae) in Rivers of Ehime Prefecture, Japan

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1 Biogeography Aug. 20, 2010 Occurrence and Habitats of the Giant Mottled Eel Anguilla marmorata (Anguilliformes, Anguillidae) in Rivers of Ehime Prefecture, Japan Kouki Mizuno 1,2 and Kazuya Nagasawa 2* 1 Ehime Prefectural Uwajima Fishery High School, Meirin, Uwajima, Ehime, Japan 2 Graduate School of Biosphere Science, Hiroshima University, Kagamiyama, Higashi-Hiroshima, Hiroshima, Japan Abstract. Japan is the northernmost distributional area for the giant mottle eel Anguilla marmorata Quoy & Gaimard, A total of 45 giant mottled eels were collected with eel pots from July 1997 to March 2010 in the freshwater lower reach of the Renjoji River in Ehime Prefecture, Shikoku Island, Japan. The number of A. marmorata caught per year was up to 11 (mean 3.4), indicating that the species was in quite low abundance in this river. Most of the eels were captured from June to September. Some eels were also captured incidentally in three adjacent rivers. The eels caught in the Renjoji River were small ( cm in total length), which was probably caused by the selectivity of fishing gear used. As the eels were mainly captured at sites covered with emergent plants and inhabited by decapod crustaceans and fishes, such environment may be suitable for the habitats of A. marmorata. Key words: Anguilla marmorata, seasonal occurrence, body size, habitats Introduction The giant mottled eel Anguilla marmorata Quoy & Gaimard, 1824 is a tropical anguillid that grows up to almost 180 cm in total length and 28 kg in body weight (Williamson & Boetius, 1993). This species occurs in freshwater in a wide region of the Indo-Pacific region, ranging from South Africa and Madagascar through the coast of Southeast Asian countries to China, Taiwan, South Korea and Japan (Watanabe et al., 2009). It also occurs in oceanic islands, such as Palmyra Atoll and the Marquesas Islands in the central Pacific and the Galápagos Islands in the eastern Pacific (Williamson & Boëtius, 1993; Handler & James, 2006; Watanabe et al., 2009). The biology of A. marmorata is very poorly known * Corresponding author: ornatus@hiroshima-u.ac.jp in Japan. Recently, based on the literature published from 1963 to 2009, Mizuno & Nagasawa (2009) compiled information on the current geographical distribution of the species in Japan and reported that it mainly occurs in the regions along the coasts facing the North Pacific and the East China Sea and in southern small islands, including the Ryukyu Islands and the Bonin (Ogasawara) Islands: this distributional pattern is strongly affected by the route of the Kuroshio. Yamamoto et al. (2001) found that the glass eels of A. marmorata migrated to waters around Yaku Island, southern Japan, with peaks in June and September. Arai et al. (2002) also estimated the timing and duration of metamorphosis of the glass eels and the age at their recruitment to waters of the nearby Tanegashima Island. Currently, Chino & Arai (2009) reported the migratory history of the species in the Bonin Islands by studying strontium and calcium concentrations in 133

2 Occurrence and Habitats of Anguilla marmorata in Rivers of Ehime Prefecture Fig. 1. A map of southwestern Ehime Prefecture, Shikoku Island, showing the sampling sites (closed circles) of Anguilla marmorata in the Renjoji, Sodu, Nagasu, and Nakajitsu rivers. The sampling location in the Iwamatsu River, where the species was collected by Ito & Mizuno (1978), is indicated by an open circle. otoliths. Since 1997, we have conducted research on the biology of two freshwater eels, A. marmorata and the Japanese eel Anguilla japonica Temminck & Schlegel, in Ehime Prefecture, Shikoku Island, Japan (Mizuno et al., 2000). In this prefecture, A. marmorata has been registered as a vulnerable species that is supposed to be facing a high risk of extinction in the wild (Mizuno, 2003). Our data are still quite limited but may be useful for understanding of the biology of A. marmorata for its conservation. We herein report that A. marmorata occurs in low abundance throughout the year at freshwater sites with emergent plants in the Renjoji River and adjacent rivers, Ehime Prefecture. Ecological aspects of A. japonica concurrently occurring with A. marmorata will be reported elsewhere. Materials and Methods Freshwater eel sampling was conducted with the assistance of a fisherman (Mr. Susumu Takamori) in the lower reach of the Renjoji River (32 57 N, E at the mouth), Ainan, southern Ehime Prefecture, from July 1997 to March 2010 (Fig. 1). The river is short (3.8 km long), flowing into Misho Cove connected to the Bungo Channel (the western North Pacific Ocean). Two types of fishing gear, eel pots (locally called unagi-jigoku, cm long and cm in diameter) and eel tubes ( korogashi, 100 cm long and 5.0 cm in diameter), were employed to catch eels. The eel pot is a polyvinyl-chloride (PVC) pipe and has a funnel-shaped bamboo cap and a plastic net (mesh size=10 [rarely 5] mm) at the anterior and posterior ends, respectively. The eel tube is also a PVC pipe but has no cover at both ends. Two eel tubes were usually set as a pair. Approximately 10 live freshwater shrimps, 134

3 Kouki Mizuno and Kazuya Nagasawa Fig. 2. A map of the lower reach of the Renjoji River, showing the sites where Anguilla marmorata was collected (open rectangles) and not collected (closed circles). As the collection sites were often overlapped, the number of open rectangles was fewer than the actual number of catch. Note no collection of A. marmorata in the brackish-water region. such as Macrobrachium japonicum (De Haan) and M. nipponense (De Haan) (Decapoda, Palaemonidae), were placed in each eel pot, but no bait was used for the eel tubes. Although the number of eel pots used was different between seasons, up to 29 and 23 eel pots were widely set in the brackish-water (ca m from the mouth) and freshwater regions (ca 630 1,650 m from the mouth), respectively (Fig. 2). Similarly, up to 19 and 33 pairs of eel tubes were set in each of these regions. The fishing gear was examined by Mr. S. Takamori for fish entrapment once a day or every two days in the warm-water season (from mid-may to late October) but once a week in other seasons. When A. marmorata was trapped, specimens were sent to the senior author (KM) to examine their morphology including total length (TL, cm) measurement. From July 2007 to October 2009, the senior author joined Mr. S. Takamori in fishing once to three times per month to record the number of both A. marmorata and A. japonica caught and also measured surface water temperature in the freshwater region. In addition, the presence of aquatic plants and animals as possible prey for A. marmorata was examined in the freshwater and brackish-water regions. Furthermore, incidental catches of A. marmorata in other rivers (Nagasu River, Sodu River, and Nakajitsu River, Fig. 1) adjacent to the Renjoji River were recorded, and the eels caught were measured for TL. Twelve specimens of A. marmorata have been deposited in the fish collection at the Tokushima Prefectural Museum, Tokushima, Japan (TKPM-P , 13171, 13205, 13608, from the Renjoji River; TKPM-P6364 from the Sodu River; TKPM-P13607 from the Nakajitsu River). Results Occurrence of Anguilla marmorata in the Renjoji River Forty-five specimens of A. marmorata were collected in the Renjoji River during a period from July 1997 to March Of these, 44 fish were trapped with the eel pots and one fish was found dead on March 15, There was no catch by the eel tubes. The abundance of A. marmorata was very low: the number of fish caught per year ( ) ranged from 0 to 11 (mean 3.4) (Table 1). In addition, from July 2007 to October 2009, a marked difference was found in abundance between A. marmorata (N=1) and A. japonica (N=74). Specimens of Anguilla marmorata were taken only in the freshwater region (Fig. 2), while those of A. japonica were collected in the freshwater and brackishwater regions (N=32 and 42, respectively, from July 2007 to October 2009). The sites where A. marmorata was caught were mostly covered with emergent plants, such as Phragmites australis (Cav.) (Poales, Poaceae) 135

4 Occurrence and Habitats of Anguilla marmorata in Rivers of Ehime Prefecture Table 1. Total length distribution of specimens of Anguilla marmorata caught in the Renjoji River, Ehime Prefecture, Japan. Total length (cm) Year ³60 unmeasured Total 1997 * * ** 1 Total * The data for 1997 and 1998 are from Mizuno et al. (2000). ** This fish was not trapped but found dead. Table 2. Monthly changes in number of Anguilla marmorata caught with eel pots in the Renjoji River, Ehime Prefecture, Japan. Month Year Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Total 1997 * * ** 1 Total * The data for 1997 and 1978 are from Mizuno et al. (2000). ** This fish was not trapped but found dead. and Sparganium japonicum Rothert (Typhales, Sparganiaceae) (Fig. 3). Near these plants, springwater was also found, and shrimps (Macrobrachium japonicum and M. nipponense), crabs (Chiromantes dehaani (H. Milne Edwards) and Eriocheir japonicus (De Haan) [Decapoda, Grapsidae]) and fishes (Nipponocypris temminckii (Temminck & Schlegel), Tribolodon hakonensis (Günther) [Cypriniformes, Cyprinidae], Oryzias latipes (Temminck & Schlegel) [Beloniformes, Adrianichthyidae], Eleotris oxycephala Temminck & Schlegel [Perciformes, Eleotridae], Luciogobius guttatus Gill, and Rhinogobius spp. [Perciformes, Gobiidae]) were abundantly found. The bottom consisted of mud and small pebbles. By contrast, in the brackishwater region where A. marmorata was not captured, there were no emergent plants, and the bottom was mainly composed of fist-sized rocks. Some shrimps (M. japonicum and M. nipponense, and Palaemon spp. [Decapoda, Palaemonidae]), crabs (C. dehaani, E. japonicus, Hemigrapsus penicillatus (De Haan), and 136

5 Kouki Mizuno and Kazuya Nagasawa Fig. 3. A picture of the lower reach of the Renjoji River, showing the emergent plants covering the sampling location. The picture was taken on April 29, H. sanguineus (De Haan) [Decapoda, Grapsidae]), and fishes (Redigobius bikolanus (Herre), Glossogobius olivaceus (Temminck & Schlegel), Acanthogobius flavimanus (Temminck & Schlegel) [Perciformes, Gobiidae]) were less abundantly found. Most specimens (N=41, 93.2%) of A. marmorata were trapped from June to September (Table 2). These fish were small, measuring 30.3 to 59.7 (mean 46.9, N=25) cm TL (Table 1), whereas one fish found dead on March 15, 2010 was much bigger (113.0 cm TL). There was a seasonal fluctuation in water temperature in the freshwater region of the river: the highest (25.7 C) and lowest (13.9 C) temperatures were recorded in July 2008 and March 2009, respectively (Fig. 4). Occurrence of Anguilla marmorata in other rivers Seven specimens of A. marmorata were incidentally captured in three rivers (Nagasu River, Sodu River, Nakajitsu River) near the Renjoji River. Five fish were caught in the Nagasu River (with eel pots): two (41.2 and 57.0 cm TL) and one (36.8 cm TL) were taken in June and July 2007, respectively, and two (38.3 and 54.5 cm TL) were collected in July Two fish (43.7 and 30.8 cm TL) were each captured in the Sodu River in July 1998 (with an eel pot) and in the Naka- jitsu River in July 2001 (with a scoop net). All these fish were caught in the freshwater region (ca 500, 1000, and 500 m upstream from the mouth of the three rivers, respectively). The collection sites in the Nagasu and Sodu rivers were covered with emergent plants, like in the Renjoji River, whereas that in the Nakajitsu River was less thickly covered with those plants. Discussion Despite an over 14-year survey, only 45 specimens of Anguilla marmorata were collected in the Renjoji River: the mean number of eels trapped per year was as low as 3.4. This low abundance of the species can be explained by two possible reasons: small recruitment to the river, and selectivity of fishing gear used (see below). Since the study location is situated as the almost northern limit of the distribution for the species, the abundance of its recruitment is most likely to be low. The species so far has been regarded as being rare in Shikoku Island (Ochiai et al., 1979; Mizuno, 2003). The specimens of A. marmorata were mainly caught from June to September in the Renjoji River. The species was also collected in June and July in three other rivers near the Renjoji River. Mizuno & Nagasawa 137

6 Occurrence and Habitats of Anguilla marmorata in Rivers of Ehime Prefecture Fig. 4. Monthly changes in surface water temperature in the freshwater lower reach of the Renjoji River from July 2007 to October (2009, table 1) reported a similar seasonal catch of the species, based on the data of catches in 10 prefectures in Japan including Ehime Prefecture. These seasonal variations in catch appear to be related to seasonal fluctuations in activity of the species. In the Renjoji River, water temperature was high (up to 25.7 C) during the summer months, when the species can be more active than in other months. In addition, water temperature remained high (more than 13.9 C) even in the winter months, which is most probably caused by the presence of springwater. This condition can allow the tropical anguillid A. marmorata to overwinter in the rivers in southern Shikoku which are located in the temperate region. In this study, we collected A. marmorata in the freshwater region of the Renjoji River and the three adjacent rivers. A similar freshwater residence of the species has been reported from rivers in Taiwan and the Philippines (Shiao et al., 2003; Briones et al., 2007). We also confirmed that, in the Renjoji River, another anguillid species A. japonica was also present and more abundant than A. marmorata. Within this river, A. japonica was more abundant in the brackish-water region than in the freshwater region. Nishi & Imai (1969) reported that these species segregated their habitats in the Isso River, Yakushima Island, southern Japan. Shiao et al. (2003) also found that the two species used different habitats in the same river in Taiwan: A. marmorata and A. japonica are more abundant in the upper and lower reaches, respectively. From these observations, Shiao et al. (2003) suggested that both interspecific competition and adaptive radiation occur between the two species. While Japan is the northernmost distributional area for A. marmorata, it may be probable that similar habitat segregation exists between them even in rivers of this country. We need more information on the migratory behaviors, microhabitats, and feeding habits of these species in Japanese rivers. The specimens of A. marmorata captured in the Renjoji River were all small ( cm TL). This was probably caused by the use of eel pots with short length and small diameter (65 80 cm long and cm wide). In addition, there was no catch of A. marmorata by the eel tubes, which may have been partly caused by the fact that no bait was placed in them. A dead specimen of A. marmorata measuring cm TL was found in the river, which indicates that largesized eels are present as well. More information on the distribution and abundance of such large eels is necessary based on catches using different types of fishing gear. The sites where A. marmorata was collected in this study were commonly covered with the emergent plants. We think that such sites can provide the eels with excellent habitats for their feeding, because their possible prey (freshwater shrimps, crabs, and fishes) was abundantly found. Freshwater crabs are known to be one of the major prey animals eaten by A. marmorata (e.g. 138

7 Kouki Mizuno and Kazuya Nagasawa Williamson & Boëtius, 1993). Since we have not yet examined the stomach contents of the species in the study area, we need clarify its feeding habits. Also, in order to keep the populations of A. marmorata stable in the rivers, it is important to conserve those areas that are covered with emergent plants and abundantly inhabited by decapod crustaceans and fishes. Acknowledgements We thank Mr. Susumu Takamori and his family, Ainan, Ehime Prefecture, and Mr. Hirotaka Katahira, Hiroshima University, for assistance in sampling. Thanks also go to Mr. Kiyokazu Hashigoe, Ehime Prefectural Ozu High School for useful information on the vegetation of the Renjoji River. We are grateful to an anonymous reviewer for constructive comments on the manuscript of the paper. References Arai, T., Marui, M., Otake, T. & Tsukamoto, K., Inshore migration of a tropical eel, Anguilla marmorata, from Taiwanese and Japanese coasts. Fish. Sci., 68: Briones, A. A., Yambot, A. V., Shiao, J. C., Iizuka, Y. & Tzeng, W. N., Migratory pattern and habitat use of tropical eels Anguilla spp. (Teleostei: Anguilliformes: Anguillidae) in the Philippines, as revealed by otolith microchemistry. Raffles Bull. Zool., Suppl., 14: Chino, N. & Arai, T., Migratory history of the giant mottled eel (Anguilla marmorata), in the Bonin Islands of Japan. Ecol. Fresh. Fish. 2010, 19: Handler, A. & James, S. A., Anguilla marmorata (giant mottled eel) discovered in a new location: natural range expansion or recent human introduction? Pac. Sci., 60: Ito, T. & Mizuno, N., River Ecology Focusing on the Fishes of the Iwamatsu River System, and Assessment of the Impact of Dam Construction. 97 pp., 7 pls., Fisheries Resource Research Group for the Iwamatsu River System, Matsuyama. (In Japanese). Mizuno, K., Giant mottled eel Anguilla marmorata. In The Committee of Valuable Wild Animals and Plants of Ehime Prefecture (Ed), Red Data Book EHIME: Threatened Wildlife of Ehime Prefecture: 104. Ehime Prefectural Government, Matsuyama. (In Japanese). Mizuno, K. & Nagasawa K., The current status of the geographical distribution of the giant mottled eel Anguilla marmorata (Anguilliformes, Anguillidae) in Japan. Bull. biogeogr. Soc. Japan, 64: (in Japanese with English abstract). Mizuno, K., Shimizu, T., Yamamoto, T. & Koyano, T., Record of the marbled eel, Anguilla marmorata, from perimeter of the Uwa Sea, southwestern part of Shikoku Island, Japan. Bull. Tokushima Pref. Mus., 10: (in Japanese with English abstract). Nishi, G. & Imai, S., On the juvenile of Anguilla marmorata Quoy et Gaimard in Yakushima (Yaku Island). Its ecology and morphology. Mem. Fac. Fish., Kagoshima Univ., 18: (in Japanese with English abstract). Ochiai, A., Teraoka, K. & Hanzawa, N., A survey of freshwater fishes of Kochi Prefecture. Res. Rep. Kochi Univ., Agr. Sci., 28: (in Japanese with English abstract). Shiao, J. C., Iizuka, Y., Chang, C. W. & Tzeng, W. N., Disparties in habitat use and migratory behavior between tropical eel Anguilla marmorata and temperate eel A. japonica in four Taiwanese rivers. Mar. Ecol. Prog. Ser., 261: Watanabe, S., Miller, M. J., Aoyama, J. & Tsukamoto, K., Morphological and meristic evaluation of the population structure of Anguilla marmorata across its range. J. Fish. Biol., 74: Williamson, G. R. & Boëtius, J., The eels Anguilla marmorata and A. japonica in the Pearl River, China, and Hong Kong. Asian Fish. Sci., 6: Yamamoto, T., Mochioka, N. & Nakazono, A., Seasonal occurrence of anguillid glass eels at Yakushima Island, Japan. Fish. Sci., 67: (Accepted 20 July, 2010) 139